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On the Taxonomic Recognition of Skinks from the Guadeloupe Archipelago (Squamata, Mabuyidae, Mabuya)

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On the Taxonomic Recognition of Skinks from the Guadeloupe Archipelago (Squamata, Mabuyidae, Mabuya) caribbean herpetology article On the taxonomic recognition of skinks from the Guadeloupe Archipelago (Squamata, Mabuyidae, Mabuya) S. Blair Hedges1,*, Olivier Lorvelec2, 3, Nicolas Barré3, Nicolas Vidal4, and Claudie Pavis3 1Center for Biodiversity, Temple University (502 SERC), 1925 N. 12th Street, Philadelphia, PA 19122, USA. 2INRA, UMR0985 Écologie et Santé des Écosystèmes, Agrocampus ouest, 35042 Rennes Cedex, France. 3AEVA, Association pour l’Étude et la protection des Vertébrés et végétaux des petites Antilles, 97170 Petit Bourg, Guadeloupe, France. 4ISYEB, UMR7205 MNHN-CNRS-UPMC-EPHE, Muséum National d’Histoire Naturelle, Département Systématique et Evolution, CP30 25 rue Cu- vier 75005 Paris, France. *Corresponding author ([email protected]) Edited by: Robert W. Henderson. Date of publication: 6 March 2019. Citation: Hedges SB, Lorvelec O, Barré N, Vidal N, Pavis C. 2019. On the taxonomic recognition of skinks from the Guadeloupe Archipelago (Squamata Mabuyidae, Mabuya). Caribbean Herpetology 64:1–7. DOI: 10.31611/ch.64 Abstract The six species of mabuyid lizards (skinks) of the Guadeloupe Archipelago are Capitellum mariagalantae, Mabuya cochonae, M. desiradae, M. grandisterrae, M. guadeloupae, and M. parviterrae. All are critically en- dangered and four may be extinct, primarily from predation by introduced mammals. These six species were described in recent years from molecular and morphological analyses. Miralles et al. (2017, Bulletin de la Société Herpétologique de France, 163, 67–84) has challenged the taxonomy, claiming that the six species cannot be diagnosed from each other, and recognized only a single species, Mabuya desiradae. We find that their study contains errors that led them to that incorrect conclusion, including a probable data handling error in the molecular analysis and the use of non-diagnostic morphological characters. Keywords: Caribbean, island, lizard, phylogeny, Mabuya, conservation, systematics. Introduction Skinks of the lizard family Mabuyidae occur throughout the Caribbean region and are especially diverse in the Guadeloupe Archipelago, where six named species occur, all endemic to individual islands: Capitellum mariaga- lantae, Mabuya cochonae, M. desiradae, M. grandisterrae, M. guadeloupae, and M. parviterrae (Hedges & Conn 2012; Hedges et al. 2016). They are critically endangered species primarily because of predation by introduced mam- mals, especially the Small Indian Mongoose, Urva auropunctata. Only two of the species, M. desiradae (from La Désirade) and M. parviterrae (from Terre de Bas, Îles de la Petite Terre), have been observed in recent years. The species M. parviterrae is particularly threatened, with an estimated 50 individuals surviving primarily in a single stone wall (Hedges et al. 2016). Additional surviving populations of skinks in the Guadeloupe Archipelago, not yet assigned to a species, occur on the small islets of Les Saintes, specifically from Terre-de-Haut and Terre-de-Bas (Angin & Gomès 2015; Barré et al. 2016). Before 2012, there was little concern for these lizards from Guadeloupe because they were thought to belong to a single, wide-ranging species, Mabuya mabouya, as concluded by studies of morphological and molec- ular data (Miralles 2005; Miralles et al. 2009). However, Hedges & Conn (2012) came to a different conclusion after conducting a comprehensive study utilizing new molecular data, together with a greatly-expanded morpholog- ical data set (30 characters) scored from 750 specimens, compared with 311 specimens in the previous work. The Hedges & Conn (2012) study revealed a hidden diversity of skink species in the Western Hemisphere and especially 1 Caribbean Herpetology, 64,1–7 ISSN 2333-2468 www.caribbeanherpetology.org caribbean herpetology article on Caribbean islands. As part of that work, they described five of the six known species in the Guadeloupe Archi- pelago, with M. parviterrae described later (Hedges et al. 2016). Recently, Miralles et al. (2017) revisited the taxonomy of skinks in the Guadeloupe Archipelago with new sequence data from seven specimens representing two of the six named species (M. desiradae and M. parviterrae), including three individuals from Les Saintes (two from Terre-de-Haut and one from Terre-de-Bas) that are unas- signed to a species. They combined those data with published sequence data (Hedges et al. 2016) from 12 speci- mens of those species (two from La Désirade and ten from Îles de la Petite Terre), concluding that the molecular ev- idence supports the recognition of a single species (Mabuya desiradae) from the Guadeloupe Archipelago instead of six species. Oddly, their resulting tree of relevance (Miralles et al. 2017: Fig. 2D) supported the opposite conclu- sion, showing that the two species formed strongly-supported genetic groups, except for a single individual from La Désirade that was genetically identical to M. parviterrae. We consider the latter to be a data-handling error made by those authors (see below). The new morphological data taken by Miralles et al. (2017) were irrelevant because they failed to score characters determined to be diagnostic in previous studies (see below). Here, we examine the study of Miralles et al. (2017), showing that it contains errors and inconsistencies and draws conclusions that are unsupported by their own data. Most (seven) of the 11 new sequences contributed by Miralles et al. (2017) (their Table 1, in bold) were from a conserved gene, 12S rRNA, with only four new cytochrome b sequences. Because our data (Hedges et al. 2016) were from the more relevant cytochrome b gene, we corrected this imbalance by adding new 12S rRNA sequences for our 12 samples in order to have an alignment of 17 individuals for both genes. Methods All methods followed Hedges & Conn (2012) and Hedges et al. (2016), including the tree analysis methods (max- imum likelihood GTR + gamma model and 2000 bootstrap replications, and Bayesian analysis with MCMC chain- length of 50,000,000. The 11 new sequences of 12S rRNA were deposited in Genbank (MK423217–MK423227, MK432848) and added to cytochrome b sequences from Hedges et al. (2016) (Genbank KU587588–KU587599) and 8 sequences contributed by Miralles et al. (2017): Genbank KT351073–074, KT351076–077, KT351079–82. We did not use sequences from several individuals (PT6–PT7, TdB1) in Miralles et al. (2017) for our phylogenetic analysis because they were from the conserved 12S rRNA gene; the relevant variable gene, cytochrome b, was not sequenced by those authors in those individuals. Most of the new sequences are of Mabuya parviterrae (SBH 274694–695, 274765–772) from Îles de la Petite Terre, Terre de Bas (16.169, -61.121). One (SBH 274696) is from La Désirade, Baie Mahault (16.331, -61.017) and another (SBH 274777) is from La Désirade; Beausejour (16.304, -61.072). See Genbank numbers (Genbank 2019) for complete localities and coordinates. Museum and laboratory voucher abbreviations are KU (University of Kansas, Natural History Museum), MNHN (Muséum National d’Histoire Naturelle, Paris), and SBH (Laboratory of S. Blair Hedges, Temple University); some Genbank accession numbers, coincidentally, begin with “KU” but are so indicated. Results and Discussion The molecular evidence. The only relevant molecular analysis in Miralles et al. (2017) was that of cytochrome b sequences in Guadeloupe skinks, rooted with the closest relative M. dominicana, which was done by those au- thors (Miralles et al.: Fig. 2D). This is because cytochrome b, and other protein-coding mitochondrial genes, evolve several times faster than 12S rRNA, providing the needed variation for closely related species, and sequences of that gene are available for most (16 of the 19) sampled individuals from Guadeloupe, compared with only seven sequenced individuals for 12S rRNA. The most relevant analysis of Miralles et al. (2017) shows strong support for the monophyly of skinks from different islets of Guadeloupe, justification for recognition of the species diagnosed by Hedges & Conn (2012) and Hedges et al. (2016), pertinent here: M. desiradae and M. parviterrae. This is not sur- 2 Caribbean Herpetology, 64,1–7 ISSN 2333-2468 www.caribbeanherpetology.org caribbean herpetology article prising because most of the sequences of those two species, used by Miralles et al. (2017), were produced and an- alyzed in those two earlier studies. Our new tree (Fig. 1) fills in the missing 12S rRNA data and confirms that result. In particular, it shows again the differentiation of skinks from three islets of the Guadeloupe Archipelago and the anomalous specimen “Des2” from the study of Miralles et al. (2017). This brings us to the conundrum: why Miralles et al. (2017) concluded the opposite of what they demon- strated (their Fig. 2D). They claimed that they were “unable to find any differentiation between the different pop- ulations of the islands of Guadeloupe.” As noted above, the 12S rRNA data they presented (e.g., their Fig. 2C) are not relevant because they are too slow-evolving and there are too few sequences. Although not stated by them, the answer must lie in that one problematic specimen, their “Des2” = “Désirade (a)” in Fig. 2 of Miralles et al. (2017) from La Désirade, which does not group with the other three individuals from that island but instead is genetically identical to the 10 individuals of M. parviterrae. Their hypothesis, apparently, is that the two islands are occupied by a single species and therefore the mixing of haplotypes on multiple islands supports that hypothesis. However,
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